Selection criteria
Obviously, to conduct a breeding programme, clear selection criteria are required.
The acetylene reduction assay was frequently used as a selection criterion in breeding for improved N2-fixation in the past, but the method is now known to be inaccurate.
The extent of nodulation, assessed as nodule number, nodule mass or simple nodule scores, has also been used as a criterion and is sometimes correlated with total N2
fixed, at least in soils poor in N. Total N accumulation, which is a good indication of the total amount of N2fixed, at least in soils with a poor capacity to supply combined N (Chapter 4), is probably the best broad criterion for selection programmes in the tropics. In soybean, ability to fix N2appears to be closely related to early formation of nodules, a simple criterion which could be used in breeding (Pazderniket al., 1996, 1997a,b).
A large number of plant characters contribute to N2-fixation and it is thus important to clarify whether the plant selection can discriminate between plants with a real ability to nodulate and fix N2better consistently in the field and plants that are simply more vigorous, and thus nodulate better, under a given environment. Genetic adaptation to specific environments can complicate the selection of genotypes with enhanced N2-fixation. This is particularly apparent in P. vulgaris. Rio Tibagi, a genotype considered to have a poor capacity to nodulate and fix N2in Brazil (Duque et al., 1985), nodulates and fixes N2 as well as some of the genotypes specifically selected for N2-fixation in Colombia (Kipe-Nolt and Giller, 1993). The genotype Puebla 152, which nodulates profusely in Colombia and has been used as a parent line with good nodulation in breeding for enhanced N2-fixation (Rosas and Bliss, 1986), was found to be among the poorest nodulators when many genotypes of P. vulgariswere compared in Queensland, Australia (Reddenet al., 1990). This is perhaps not surprising given the enormous breadth of environmental adaptation withinP. vulgaris, but it emphasizes the need either to breed specifically for local environments, or to screen genotypes across the wide range of environmental conditions that they are likely to encounter in the field. This is especially true given the unpredictability of the climate in many parts of the tropics.
Effects of intercropping on N2-fixation
Often the overall benefit of growing two crops in a mixture will be a net benefit in which the increase in growth of one crop exceeds a small competitive reduction in the growth of the other (Willey, 1979) and this is often seen where a low-growing legume is intercropped with a tall cereal. For example, nodulation and N2-fixation of groundnut were greatly reduced when it was intercropped with maize, sorghum or millet (Nambiaret al., 1983a). Similarly, growth and N2-fixation of soybean were reduced by a tall sorghum intercrop, whereas N2-fixation per plant was enhanced by a dwarf sorghum (Wahua and Miller, 1978), indicating that the reduction in yield and N2-fixation was partly caused by shading. Studies using the15N isotope dilution method indicated that, although the total amount of N2 fixed was substantially reduced from 97 to 62 kg N ha-1in ricebean (V. umbellata) intercropped with maize, the proportion of N derived from N2-fixation in the ricebean was increased from 72% to 90% (Rerkasem and Rerkasem, 1988). This increase in the proportion of N from N2-fixation in the legume was due to efficient depletion of mineral N from the soil by the cereal crop, thus reducing nitrate-induced suppression of nodulation (Chapter 3). However, experiments using similar methods with maize/cowpea intercrops found no such effects on N2-fixation (Oforiet al., 1987; Van Kessel and Roskoski, 1988). Some caution must be exercised in drawing conclusions from isotope dilution experiments as the differences in15N-enrichment used to calculate N2-fixation may be due either to competition for soil N in the intercrops or to differ- ent15N uptake patterns between crops (Abaidoo and van Kessel, 1989) (Chapter 4).
Competition for soil N between cereal crops and legumes often results in the legume deriving a greater proportion of its N from N2-fixation, as demonstrated with pigeonpea/cereal intercrops (Tobitaet al., 1994; Sakalaet al., 2001). The extent to which growth and the total amount of N2fixed by the legume crop is decreased in the intercrop depends on the degree of complementarity between the crops. A much quoted example of the benefits of intercropping legumes and cereals is that of pigeonpea intercropped with maize or sorghum (Dalal, 1974; Onget al., 1996). The early growth of pigeonpea is very slow so that it affords little competition and yields of the cereal crop are unaffected (Sakalaet al., 2001). When intercropped with maize or short-duration varieties of sorghum, pigeonpea continues to grow on residual soil moisture long after the cereal crop has been harvested, and the amounts of N2fixed by pigeonpea are the same when grown in mixture or as sole crops (Sakalaet al., 2001).
As discussed in Chapter 5, there is little evidence for direct transfer of significant amounts of N between roots of legumes and cereals in mixtures, and this conclusion is supported by measurements of natural15N abundance in intercrops of pigeonpea and sorghum (Tobitaet al., 1994). Although pigeonpea loses large amounts of N in leaves that fall during crop growth, these cause an initial immobilization of soil N when they decompose and so little of the N is available for use by intercropped cereals (Sakalaet al., 2000). The available evidence indicates that inputs of fixed N are more likely to benefit subsequent crops (see below).
Although intercrops can produce greater yields, they generally do so by extract- ing more nutrients from the soil than sole crops (Dalal, 1974; Masonet al., 1986) and may therefore cause more rapid decline in soil fertility. Similarly, intercrops use more water for growth: when rainfall was adequate a cowpea/maize intercrop gave superior crop yields, but competition for moisture in a drought year caused drastic reductions in yields of intercropped maize (Shumbaet al., 1990).
Net N benefits and residual effects of grain legumes
Substantial quantitative information on the amount of N available to crops succeed- ing legumes in a rotation – that is, on the residual effect of the legume – is available (Table 8.4). The beneficial effects of legumes on succeeding crops can often arise due to a variety of other effects, such as reduction of disease incidence (e.g. Marcellos et al., 1997), or by reducing attack by striga, a parasitic weed that can often devastate yields of cereal crops (Reddyet al., 1994), as well as other changes in soil fertility (see Table 5.2). These other ‘rotation effects’ must also be considered when assessing the benefits from N2-fixation in crop rotations.
Net N benefits of grain legumes
For grain legumes to play an important role in the maintenance of soil fertility for other crops in the rotation, they must obviously leave behind more N from N2-fixation than the amount of soil N that is removed in the crop. Clearly the two purposes served by the crop – one to provide grain yield and the other to leave residual N – are somewhat contradictory. The role of grain legumes in contributing N to cropping systems is bound, therefore, to be compromised by the breeding priority of optimizing the efficiency of conversion of N into the grain removed (Henzell and Vallis, 1977). The amounts of N added to the cropping system that have been measured are very variable for all of the main species on which there is substantial information (Table 8.4). In many cases there is no net benefit from including a grain legume in the crop rotation, even when the legume stover is returned to the field. The largest net benefits tend to be found with groundnut and cowpea, as at least some varieties of these crops generally have a smaller N harvest index (NHI). However, some newer varieties of groundnut have higher yield potential and larger NHI as a result (Bellet al., 1994). The ‘hay’ or fodder varieties of cowpea and soybean produce large amounts of stover. The promiscuously nodulating variety ‘Magoye’ yielded over 10 t of stover ha-1 when grown on a fertile soil in Zimbabwe, containing almost 140 kg N ha-1(Kasasaet al., 1999). Similarly, lablab (L. purpureus), a relatively ‘unimproved’ legume with vigorous vegetative growth and poor grain yield, generally left more residual N than groundnut, soybean or pigeonpea (MacColl, 1989). If the legume stover is removed from the field, the net effect of growing a legume crop on the N balance of the cropping system is always negative unless contributions from fallen leaves, roots and nodules is considered.
Based solely on above-ground plant parts, the net loss of N from the system from growing grain legumes can easily be 100 kg N ha-1or more.
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Chapter 8 Grain legume
Duration (days)
Grain yield (t ha-1)
Stover yield (t ha-1)
Harvest index
(%)
% N from N2-fixation
(%)
Amount of N2fixed (kg N ha-1)
N in stover (kg N ha-1)
N harvest index
(%)
Net input from N2-fixation (kg N ha-1)
Recovery of stover N (%)
Residual effect in fertilizer equivalents
(kg N ha-1) Refsa
Arachis hypogaea Cajanus cajan Cicer arietinum Glycine max Phaseolus vulgaris Vigna radiata Vigna unguiculata
90–140 90–241 140–175 96–104 72–114 70–84 69–115
0.3–3.1 0.2–1.4 0.6–2.9 0.8–3.0 0.1–4.0 0.7–1.7 0.2–2.7
1.4–6.7 1.8–13.8 5.9–7.5 1.0–10.4 0.1–7.5 1.3–3.9 1.0–8.4
25–47 8–54 23–78 16–57 21–64 28–46 9–42
16–92 0–88 0–96 12–100
0–73 0–100 32–76
21–206 0–166 0–124 26–188 2–125 61–107 9–201
52–166 12–50
– 30–170
3–38 30–88 20–94
30–70 21–68 43–66 37–88 44–93 54–67 29–66
-37 to 100 -32 to 41 -47 to 46 -37 to 59
– -20 to 10 -11 to 136
12–26 9–15
– 14–23
– 4–58 12–24
0–97 0–67
? 0–22
– 68–94 38–205
1 2 3 4 5 6 7
a(References in addition to those cited in Table 8.2) 1: Bandyopadhyay and De, 1986; MacColl, 1989; Anuaret al., 1995; 2: Dalal, 1974; Jones and Wild, 1975; MacColl, 1989; Cobbina, 1995; Mandimba, 1995; 3: None; 4: Wetselaar and Ganry, 1982; Suwanaritet al., 1986; Ofori and Stern, 1987; MacColl, 1989; Sisworoet al., 1990; Bergersenet al., 1992; Yinget al., 1992; Kasasaet al., 1998, 1999; 5: Jones and Wild, 1975; Davis and Garcia, 1983; Davis et al., 1984; Ssali and Keya, 1984b; 6: Bandyopadhyay and De, 1986; Senaratne and Ratnasinghe, 1995; Sharmaet al., 1996; 7: Agboola and Fayemi, 1971;
Balasubramanian and Nnadi, 1980; Ssali and Keya, 1984a; Bandyopadhyay and De, 1986; Oforiet al., 1987; Van Kessel and Roskoski, 1988; Ntareet al., 1989; Sisworoet al., 1990; Bationoet al., 1991; Franzluebberset al., 1994; Klaijet al., 1994; Reddyet al., 1994; Senaratne and Ratnasinghe, 1995.
Table 8.4. Amounts of N2fixed and contributions to soil fertility by grain legumes in the tropics grown as sole crops, if only above-ground plant parts are considered and legume stover is returned to the soil.
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Residual effects on cereal crops
In northern Nigeria, maize grain yields were found to be greater following a ground- nut crop than after crops of cowpea, cotton or sorghum. The yield increase was related to an increased availability of mineral N in the soil after groundnuts (Jones, 1974). The fact that no such beneficial effect was found after growth of cowpea in the same experiment indicates that residual effects do not always occur even with legume crops (Table 8.4). In Zimbabwe, the yield of maize was greater after bambara groundnut (7.6 t ha-1) than after groundnut (6.2 t ha-1), unplanted fallow (4.3 t ha-1) or maize (3.9 t ha-1) (Mukurumbira, 1985). Groundnut and cowpea were found to have roughly equal residual effects on the growth of a subsequent maize crop in northern Ghana, equivalent to the addition of 60 kg fertilizer-N ha-1. This was despite the fact that 68 kg N ha-1 was left behind in above-ground residues after groundnut and 150 kg N ha-1after cowpea (Dakoraet al., 1987). The residual benefit of the groundnut was additive with the application of fertilizer-N, giving an increase in yield over that in maize grown after maize even when 60 kg fertilizer-N ha-1 was applied, whilst that of cowpea was replaced by the application of N- fertilizer. This suggests that the organic residues of groundnut had additional benefits that were either not due solely to their provision of N or were due to a more efficient use of the N by maize. Direct evidence of the benefits from N2-fixation was obtained where yields of sorghum grown after nodulating varieties of chickpea were better than yields after non-nodulating chickpeas (Kumar Rao and Rupela, 1998).
As most of the above-ground parts of grain legumes are removed at harvest, residual effects must come from the below-ground parts and any leaves that fall to the soil during growth of the crop. In India, pigeonpea was found to give a residual benefit to a subsequent maize crop of 38–49 kg N ha-1(Kumar Raoet al., 1983), which was partially attributed to a contribution of N from pigeonpea leaf fall of 30–40 kg N ha-1. The amount of N in leaves that fall during growth of long- duration pigeonpea may be as much as 68–84 kg N ha-1(Kumar Raoet al., 1996b;
Sakala et al., 2001). Over 12 years, yields of sorghum were consistently higher following a sorghum/pigeonpea intercrop or than after an oilseed crop, safflower (Carthamnus tinctorius), and the soil N content had increased significantly where pigeonpea had been grown (Rego and Rao, 2000). Other legumes may also contrib- ute substantial amounts of N during crop growth; inputs of 81 kg N ha-1 were measured in leaf fall from soybean in Australia (Bergersenet al., 1992). A pigeonpea/
sorghum intercrop gave no residual N benefit (Kumar Raoet al., 1987) but a reduced but significant benefit (< 10 kg N ha-1) of soybean/maize and groundnut/maize intercrops was found elsewhere (Searleet al., 1981) – much less than the residual benefit following the sole legume crops (soybean, 46 kg N ha-1; groundnut, 54 kg N ha-1). All above-ground plant parts of the legumes were removed when they were harvested and so the residual effect must have been due to leaves lost during the growth of the legume crop, or to decomposition of roots and nodules.
Yields of maize grown after soybean on an Alfisol were increased to 2.5 to 4 t ha-1, compared with only 1.8 t ha-1 in continuous maize cropping where all the legume stover had been removed (Kasasaet al., 1999), but this may be partly due to other rotational effects than simply N2-fixation. The below-ground contribution that
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specifically came from N2-fixation in groundnut was estimated by comparing N uptake by maize following nodulating and non-nodulating varieties (McDonagh, 1993; Toomsanet al., 1995). The amounts were small, ranging from 0 to 10 kg N ha-1and included inputs from both roots and fallen leaves.
Measurements of residual benefits using15N
As stated earlier, the residual benefit does not necessarily demonstrate a contribution of N from the legume N2-fixation but could simply be due to sparing effects of soil N. There are still relatively few studies in which the sources of N for the second crop have been separated. Measurements using 15N-labelled residues of grain legumes indicate that, with a few exceptions, some 10–20% of the legume N is recovered in the first subsequent crop (Giller and Cadisch, 1995) (Table 8.4). More than 70%
of the N in shoot residues of cowpea was recovered by six successive crops in cowpea/rice/soybean or cowpea/rice/maize rotations in Indonesia and up to 27% of this was found in the first crop of rice (Sisworoet al., 1990). In experiments using the isotope dilution approach to study residual effects of pigeonpea, Kumar Raoet al.
(1987) found evidence that decomposing roots as well as the fallen leaves were sup- plying N to the subsequent crop. Recovery of N from15N-labelled roots of soybean was negligible, presumably due to their poor content of N (Bergersenet al., 1992).
As indicated, groundnut has a particularly large potential to contribute N to cropping systems if the stover is returned to the soil, for two reasons: it produces large amounts of stover; and because the crop is harvested when the tops are still green, the stover is rich in N. Up to 166 kg N ha-1in the stover of a groundnut crop grown on a farmer’s field in northeast Thailand have been recorded (Toomsan et al., 1995).
Using 15N-labelled residues the fate of the N applied in groundnut stover was followed in an upland groundnut/maize/maize cropping sequence (Fig. 8.3). In this experiment the groundnut grain contained 75 kg N ha-1, and the groundnut residue that was returned to the soil contained 120 kg N ha-1. Using15N-labelled residues, 20 kg N ha-1was recovered in the first crop; of the remaining 100 kg N ha-1, half was recovered in the surface 30 cm of the soil and roughly half was missing. The N in groundnut stover is released rapidly (McDonagh, 1993) and the N that was unaccounted for was presumed to have been lost from the cropping system, either to the atmosphere through denitrification and/or volatilization or by leaching. Of the 50 kg N ha-1that remained in the soil, 5 kg N ha-1was recovered in the second crop of maize. Groundnut yielded roughly 2 t grain ha-1in the field experiments on which this N balance was based – the average yield on smallholder farms around the world is estimated to be only 0.7 t ha-1(Freemanet al., 1999) and is often much less.
Residual benefits on farmers’ fields
Smallholder farmers invariably carry the whole shoots of grain legumes from the fields for threshing or shelling, or leave them in the fields to be grazed by livestock. In on-station trials on sandy granitic soils in Zimbabwe, the yield of maize was almost doubled, from 2.5 to 4.6 t ha-1, after a groundnut crop that yielded only 0.4 t grain ha-1, even though most of the stover was removed by cattle (Waddington and Karigwindi, 2001). Benefits were much smaller and generally insignificant on farms
of five smallholders on similar soils where yields of maize were less than 0.8 t ha-1. Researcher-managed experiments in farmers’ fields in northeast Thailand, also on very sandy soils, showed that groundnut and soybean yields of 2 t ha-1and major impacts on yields of subsequent rice were readily achievable (Toomsanet al., 1995), but with much greater inputs than normally feasible for many smallholders in terms of basal fertilizers and labour for weeding.
The major role of crop residues as dry-season fodder, either for feeding to animals in stalls or by free-grazing of animals, and the extra labour involved to incorporate grain legume stover are probably the greatest limitations to residual effects in smallholder agriculture. This must, of course, be weighed against the benefits to the farmer in terms of both animal production and the cattle manure, which is a major source of nutrients for crop production in many tropical farming systems (Gilleret al., 1997).
Conclusions
Although large differences in N2-fixation potential among genotypes have been demonstrated for many grain legumes, only a few serious attempts have been made to enhance N2-fixation in grain legumes. Many legume breeders have adopted the approach of adding large amounts of N-fertilizers to help to reduce variability in their Fig. 8.3. Fate of the N in a crop of groundnut (Arachis hypogaea) grown on a sandy soil in northeast Thailand traced using15N-labelled groundnut residues.
(From McDonagh, 1993.)
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selection plots, rather than ensuring that the plants are effectively nodulated. This approach may have resulted in selection against N2-fixation whilst selecting for other desired traits. The need of American soybean varieties grown in regions outside North America for inoculation with specific rhizobia to ensure effective nodulation can be ascribed partly to the activities of plant breeders in selecting the plant genotypes in the absence of the symbiont, but it must also be recognized that soybean is far more selective than other legumes such as cowpea in its requirements for rhizobia. Once it is possible to make inoculants of selected strains freely available for use in the tropics, it may be considered that a highly specific host is preferable.
However, given the lack of inputs commonly available to smallholders in the tropics (even inputs as inexpensive as rhizobial inoculum), legumes that fix N2and grow well without the need for inoculation are the best solution for the immediate future.
Guidelines on how best to assess the requirements of legumes for inoculation are discussed in Chapter 14.
Grain legumes can contribute large amounts of N to the soil in fallen leaves and stover that can provide N for subsequent crops, sometimes resulting in spectacular yield increases on sandy soils. If the legume stover is removed, however, there is often no observable benefit to the next crop and there is usually a net removal of N from the cropping system in the legume grain. Increases in the amount of legume N contributed through residual effects is generally possible only if grain yield of the legume is decreased. This can rarely be justified in economic terms (Schwenkeet al., 1998), but might be worthwhile for smallholder farmers in remote areas who are unable to participate in a cash economy.